Three-Dimensional Measurements of Pharyngeal Airway in
Patients with Unilateral Cleft Lip and Palate
Emiko Kimura1), Tomoko Obata1), Shuto Kitai1), Takenobu Ishii1), Teruo Sakamoto1), Miki Watanabe2), Akira Watanabe2), Masato Narita2), Yoko Nakano2), Nobuo Takano3), Kenji Sueishi1) and Yasushi Nishii1) 1) Department of Orthodontics, Tokyo Dental College,
2-9-18 Kanda-Misakicho, Chiyoda-ku, Tokyo 101-0061, Japan 2) Department of Oral and Maxillofacial Surgery, Tokyo Dental College,
2-9-18 Kanda-Misakicho, Chiyoda-ku, Tokyo 101-0061, Japan 3) Oral Cancer Center, Tokyo Dental College,
5-11-13 Sugano, Ichikawa-shi, Chiba 272-8513, Japan
Received 12 March, 2020/Accepted for publication 28 July, 2020 Published Online in J-STAGE 10 November, 2020
Abstract
The aim of this study was to investigate 3-dimensional (3D) airway volume in patients with unilateral cleft lip and palate (UCLP) using computed tomography (CT). The study population comprised 15 UCLP patients (UCLP group) scheduled to receive alveolar bone grafts and 15 with impacted teeth (control group). The clinical requirements for a CT scan were met in both groups. Measurements were recorded from 3D reconstructions of Digital Imaging and Communications in Medicine data obtained from the CT images. Airway volume, cross-sectional area, and linear and angular measurements were recorded. Airway volume and cross-sectional area showed no significant difference between the two groups. The narrowest section of the airway in the UCLP group was tighter than that in the control group, however (p=0.017). The results of this study suggest that this differ-ence in the measurements of the narrowest section of the airway is involved in the particu-lar maxillofacial morphology found in UCLP patients.
Key words: Airway volume — Cleft lip and palate — Minimum cross-sectional dimensions
Introduction
The aim of palatoplasty, an essential proce-dure in the repair of cleft palate, is to obtain improvements in speech, articulation, masti-cation, and swallowing function. The
invasive-ness of this procedure, however, is known to inhibit the growth of the maxilla9,16,17). In
patients with a small and retruded maxilla, it is necessary to expand the dental arch and induce forward growth of the maxilla. It has been suggested that this type of procedure, 213
tdc04-01_kimura.indd 213
which is aimed at countering jaw hypoplasia, should be performed in conjunction with orthodontic treatment at the appropriate time. Relatively little information on the air-way in such cases, which has a posterior loca-tion, is currently available, however. Three-dimensional (3D) morphological analysis, which has been made possible only recently due to the growing popularity of computed tomography (CT) and new types of software, has yielded information that could not hith-erto have been obtained by routine cephalog-raphy. The airway, which is enclosed in soft tissues, has a complex morphology, and such 3D morphological analysis allows consider-able information to be obtained on this struc-ture. The airway is involved in breathing, speech, and swallowing. A basic understand-ing of the airway in cleft palate patients is essential in helping to anticipate problems associated with impaired speech production or articulation, such as hypernasality, sleep apnea syndrome, or dysphagia, which are caused by impairments to this structure. Some previous research has suggested that airway volumes are smaller in cleft palate patients2,4,17).
Other studies have produced conflicting results, however5,13), which suggests that the
data are as yet insufficient for a conclusion to be drawn. Hence, the purpose of the present study was to compare 3D airway measure-ments obtained from CT scans between uni-lateral cleft lip and palate (UCLP) patients and healthy controls.
Materials and Methods
The participants included in the present study comprised a total of 30 patients visiting the Department of Orthodontics or Depart-ment of Oral Surgery at Tokyo Dental College Chiba Hospital between 2000 and 2018; patients with syndromes were excluded. A total of 15 patients were assigned to a UCLP group: the clinical requirements for a CT scan due to an alveolar bone graft were met in all these patients; the CT scan included all the areas necessary for the purposes of the study; and all were aged between 8 and 13 years. A further 15 participants were assigned to a con-trol group: the clinical requirements for a CT scan due to impacted teeth were met in all these patients; and all were aged between 8 and 14 years. Computed tomography scans
Fig. 1 A, Range of airway volume measurement; B, Total airway divided into nasopharyn-geal and oropharynnasopharyn-geal airways.
Oropharyngeal airway Nasopharyngeal airway B A 【版面】W：396 pt（片段 192 pt） H：588 pt 【本文】行数不明（手組み） 10pt 12pt 送り
【図】●図番号・タイトル・説明：11.3Q 12.7H New Baskerville ITC Std 図タイトルと説明のアキ 9Q ●タイトル折り返し：番号の後（続 く説明の先頭は字下げ不要） ●図説の幅 片段：片段固定 全段：図幅
【表】●番号・タイトル・説明：11.3Q 12.7H New Baskerville ITC Std タイトルと表のアキ 10.5Q ●罫線 表はじめのみ双罫 表中の 罫の太さ 1.411mm ●表中：11.3Q 12.7H New Baskerville ITC Std ●脚注 11.3Q 12.7H New Baskerville ITC Std 字下げなし 斜体は New Baskerville ITC Std Italic（タグは <l>） 半角ダーシは -（ハイフン）に F50：tohaba の文字スタイルをかけて作成
Fig. 2 Angle formed by Frankfurt horizontal (FH)
plane, right-side orbitale (Or), and point A, FH-Or-A (a); Angle formed by FH plane, right-side orbitale (Or), and point B, FH-Or-B (b).
a b
tdc04-01_kimura.indd 214
were obtained with the patient in the supine position. All the participants were asked to refrain from swallowing during the CT scan. Measurements were recorded from 3D recon-structions of Digital Imaging and Communi-cations in Medicine data obtained from CT images using the ProPlan CMF 1.4 software (Materialize, Leuven, Belgium). The method suggested by Mevlut et al.10) was used to
calcu-late the total airway volume from the 3D reconstruction of the pharyngeal airway: this involved using the Frankfurt horizontal (FH) plane as the superior margin; the tangent to the ventral inferior margin of the third cervi-cal vertebra parallel to the FH plane as the inferior margin; a plane that passes through the posterior nasal spine (PNS) and which is perpendicular to the FH plane as the anterior margin; and the posterior pharyngeal wall as the posterior margin. Airway volume was
divided into superior and inferior sections, termed the nasopharyngeal and oropharyn-geal airway, respectively, by a plane that passes through the PNS and anterior-most promi-nence of the first cervical vertebra (Fig. 1). The area which could be subjected to the CT scan was restricted due to concerns regarding exposure to radiation. The areas that permit measurement of the sella-nasion-point A and sella-nasion-point B angles, which are ordi-narily used to evaluate the anteroposterior relationship between the mandible and max-illa, were not included. Therefore, the angles formed by FH plane-right-side orbitale (Or)- point A (FH-Or-A) and FH-right-side Or-point B (FH-Or-B) were adopted instead (Fig. 2). Several maxillary parameters such as intermo-lar width, anteroposterior airway diameter, and vertical length of the airway were mea-sured (Table 1). The cross-sectional dimen-Table 1 Measurement parameters in control and UCLP groups
1. Intermolar width Distance between central fossae of both first maxillary molars 2. FH-Or-A (°) Angle formed by the Frankfurt (FH) plane and the plane formed
by the right Orbitale and the A point
3. FH-Or-B (°) Angle formed by the FH plane and the plane formed by the right Or and the B point
4. Anteroposterior airway diameter (cm) Distance from the posterior nasal spine (PNS) to the posterior pharyngeal wall in a plane parallel to the FH plane
5. Vertical dimension (cm) of the airway Distance from the PNS to the inferior airway margin in a plane perpendicular to the FH plane
UCLP: unilateral cleft lip and palate
【版面】W：396 pt（片段 192 pt） H：588 pt 【本文】行数不明（手組み） 10pt 12pt 送り
【図】●図番号・タイトル・説明：11.3Q 12.7H New Baskerville ITC Std 図タイトルと説明のアキ 9Q ●タイトル折り返し：番号の後（続 く説明の先頭は字下げ不要） ●図説の幅 片段：片段固定 全段：図幅
【表】●番号・タイトル・説明：11.3Q 12.7H New Baskerville ITC Std タイトルと表のアキ 10.5Q ●罫線 表はじめのみ双罫 表中の 罫の太さ 1.411mm ●表中：11.3Q 12.7H New Baskerville ITC Std ●脚注 11.3Q 12.7H New Baskerville ITC Std 字下げなし 斜体は New Baskerville ITC Std Italic（タグは <l>） 半角ダーシは -（ハイフン）に F50：tohaba の文字スタイルをかけて作成
Fig. 3 A, Cross-sectional dimensions of narrowest section calculated by software; B, Meas-urement of distance from posterior nasal spine to narrowest section of airway.
A B
tdc04-01_kimura.indd 215
sions of the narrowest part of the airway and the distance from the PNS to the tangent to the ventral inferior margin of the third cervi-cal vertebra parallel to the FH plane were measured using Dolphin 3D software (V.10, Dolphin Imaging, Chatsworth, California). The vertical distance between the PNS and the narrowest section of the airway was also measured (Fig. 3). The cross-sectional dimen-sions of the narrowest section of the airway were automatically selected and calculated by the software from a designated range.
Statistical analysis was performed using the Mann-Whitney U-test to assess differences between measurements in the UCLP and con-trol groups; the Spearman’s rank correlation coefficient was used to identify the relation-ship between total airway and various other measurements. The level of significant differ-ence was set at p <0.05; the statistical software used was SPSS version 19 (SPSS, Chicago, IL, USA).
The protocol of this study was approved by the Ethics Committee of Tokyo Dental Col-lege (approval no: 738).
Results
The mean age of the 15 participants (8 male, 7 female) in the UCLP group was 11.14±3.48 years, while that of the 15 partici-pants (11 male, 4 female) in the control group was 11.31±3.44 years. No significant age-related difference was observed between the two groups. The only parameter in which sig-nificant differences between the two groups were evident was the vertical distance between the PNS and narrowest section of the airway (Table 2). Other parameters such as intermo-lar width, FH-Or-A, FH-Or-B, anteroposterior airway diameter, and vertical length of the airway showed no significant differences. Similarly, no significant differences in volume in any section of the airway were evident between the UCLP and control groups. Total airway volume was 15.78±7.00 cm3 in the
control group and 18.08±9.05 cm3 in the
UCLP group; nasopharyngeal airway volume
Table
2
Comparison of measurements between groups
Age (y) Inter molar width (cm) FH-Or -A ( ° ) FH-Or -B ( ° ) Antero- posterior -diameter (cm) Vertical length (cm) Air way volume (cm 3) Narrowest section Naso- phar yngeal phar yngeal Total sions (cm 2) Distance (cm) Control 11.31 ± 3.44 4.60 ± 0.30 41.45 ± 2.62 40.00 ± 0.10 4.00 ± 0.63 8.21 ± 1.32 6.44 ± 2.62 9.34 ± 4.89 15.78 ± 7.00 1.20 ± 1.06 2.41 ± 1.06 UCLP 11.14 ± 3.48 4.83 ± 0.30 66.19 ± 3.52 64.44 ± 4.08 4.00 ± 0.72 7.89 ± 2.21 8.34 ± 4.14 9.75 ± 5.36 18.08 ± 9.05 1.12 ± 0.65 3.85 ± 1.91 Mann-Whitney U-test NS NS NS NS NS NS NS NS NS NS p = 0.017 UCLP: Unilateral cleft lip and palate. FHA: Angle formed by Frankfurt horizontal plane, right-side or bitale, and point A. FHB: Angle formed by FH plane, right-side or
bitale, and point B.
tdc04-01_kimura.indd 216
was 6.44±2.62 cm3 in the control group and
8.34±4.14 cm3 in the UCLP group; and
oro-pharyngeal airway volume was 9.34±4.89 cm3
in the control group and 9.75±5.36 cm3 in
the UCLP group. None of these measure-ments exhibited a significant difference between the two groups (Table 2). The cross-sectional dimension of the narrowest section of the airway was 1.20±0.45 cm2 in the
con-trol group and 1.12±0.65 cm2 in the UCLP
group; no significant difference was observed between the two groups. The vertical distance from the PNS to the narrowest section of the airway was 2.41±1.06 cm in the control group and 3.85±1.91 cm in the UCLP group, which showed that the narrowest section of the air-way in the patients in the UCLP group was situated inferior to that in those in the control group (p=0.017) (Table 2).
Thorough investigations of the relation-ships between total airway volume and various other measurements revealed a moderate correlation between age (r=0.58, p=0.02) and the cross-sectional dimensions of the nar-rowest section of the airway (r=0.70, p
<0.001) in patients in the control group; and a moderate correlation between age (r=0.70, p=0.01) and vertical length of the airway (r=0.70, p=0.01) in patients in the UCLP group (Table 3).
Discussion
Airway volume has been reported to range between 10.00 cm3 and 20.00 cm3,6,7,10,13) in
healthy individuals, and between 15.00 cm3
and 17.00 cm3 in patients with CLP4,14). Similar
results were obtained from the present study, with a mean airway volume of 15.78 cm3 in the
controls and 18.08 cm3 in the UCLP group.
These values were slightly higher in the UCLP group. Previous research has found airway volume to be lower in patients with CLP2,4,17),
but conflicting results have been obtained in other reports5,13). Some studies reported that
the sections where the airway is smaller in patients with CLP vary: for example, CLP patients showed smaller oropharynges, but not total airway4,17)or nasopharynges2). In one
previous report that found no difference in airway volumes between CLP and control groups, it was concluded that any significant difference might have been eliminated by maxillary expansion attained by use of a rapid expansion device in the patients with CLP5).
Expansion of the dental arch has been associ-ated with expansion of the nasal cavity3),
how-ever, leaving the oropharynx unaffected6,18),
and maxillary expansion is believed to have little impact on pharyngeal airway volume. Maxillary expansion can also change the shape of the airway, especially those areas located in the maxilla (the nasal cavity and posterior section of the PNS, for example).
Table 3 Correlations between total airway volume and various measurements Total
airway
volume Age
Inter-molar
width FH-Or-A FH-Or-B
Antero poste-rior diame-ter Vertical length Narrowest section
Dimen-sions tance Dis-Control r 0.58 0.47 −0.20 −0.01 −0.18 0.12 0.70 0.10 p 0.02 NS NS NS NS NS p<0.001 NS
UCLP r 0.70 0.53 0.19 0.02 0.54 0.70 0.36 −0.01
p 0.01 NS NS NS NS 0.01 NS NS UCLP: Unilateral cleft lip and palate. FH-Or-A: Angle formed by Frankfurt horizontal plane, right-side orbitale, and point A. FH-Or-B: Angle formed by FH plane, right-side orbitale, and point B.
tdc04-01_kimura.indd 217
however. Some of the participants in the pres-ent study had undergone maxillary expan-sion. To counter changes due to CLP, many patients were treated orthodontically, and preliminary orthodontic treatment is required before alveolar bone grafting, in particular.
Airway volume has been reported to increase with age in healthy individuals1,15)
due to the growth of the mandible and shrink-age of the tonsils6). Another report17), however,
found no difference in airway volume between children (aged 9–12 years) and adolescents (aged 13–17 years); and no significant differ-ence was observed in the anteroposterior location or size of the jaw in these two groups, which also suggested that there would not be any difference in airway volume10). The
posi-tion of the mandible has been reported to affect the pharyngeal airway7,8,12). In the
pres-ent study, though, airway volume increased with age in both the UCLP and control groups. The absence of a correlation with the anteroposterior position of the jaw could be a cause for the absence of a difference in airway volume.
In the present study, the cross-sectional dimensions of the narrowest section of the airway were related to the total airway volume in the control group. In contrast, the UCLP group showed no such relationship. This could be attributed to the influence of the CLP and the palatoplasty procedure. To our knowledge, no previous studies have analyzed the cross-sectional shape of the airway in UCLP patients. It can be inferred, however, that CLP and its associated surgeries would affect cross-sectional morphology. Further-more, total airway volume and the vertical length of the airway showed a correlation in the UCLP group. The vertical length of the airway showed a difference between the two groups, although this was not significant. The UCLP group showed shorter lengths than the control group, however, possibly because CLP inhibits the downward growth of the max-illa16). It can be inferred that participants
severely affected by this procedure have
observed between total airway volume and vertical length of the airway in the control group. This may be explained by individual differences in the vertical length of the airway.
This study may have had limitations due to concerns regarding exposure to radiation. Correction of the wings of the nose is often performed simultaneously when performing an alveolar bone graft. In this situation, the surgeon will require CT scans not only of the maxilla, but also of the maxillofacial area in diagnosing facial symmetry. Airway volume in UCLP patients can also be measured in such CT scans. The airway has a complicated mor-phology, so it cannot be adequately visualized using 2D technology. Computed tomography scans are indispensable in this regard.
Cheung et al.5) reported that the
cross-sec-tional dimension of the narrowest section of the airway was 1.16±0.59 cm2 in CLP cases
and 1.14±0.59 cm2 in non-CLP cases, which is
not a significant difference, and similar results were obtained in the present study as well. The present results also showed that the nar-rowest section of the airway in the patients in the UCLP group was inferior to that in those in the control group. This has been attributed to the fact that retraction of the mandible leads to narrowing of the airway in the soft palate region or root of the tongue12,15), and
changes in facial morphology, especially in CLP patients, lead to retraction of the mid-face and mandible11), thus leading to increased
narrowing of the lower airway. The narrowest section of the airway is important, as it is involved in breathing, speech, and swallow-ing, and an inferior location of the narrowest section of the airway, in particular, may be involved in sleep apnea syndrome and aspira-tion pneumonitis.
Conclusion
No difference was found in airway volume between patients in the UCLP and control
tdc04-01_kimura.indd 218
to that in those in the control group.
Acknowledgements
The authors declare no conflict of interest associated with this manuscript.
References
1) Abramson Z, Susarla S, Troulis M, Kaban L (2009) Age-related changes of the upper air-way assessed by 3-dimensional computed tomography. J Craniofac Surg 20: 657–663. 2) Aras I, Olmez S, Dogan S (2012) Comparative
evaluation of nasopharyngeal airways of uni-lateral cleft lip and palate patients using three-dimensional and two-three-dimensional methods. Cleft Palate Craniofac J 49: e75–e81.
3) Basciftci FA, Mutlu N, Karaman AI, Malkoc S, Küçükkolbasi H (2002) Does the timing and method of rapid maxillary expansion have an effect on the changes in nasal dimensions? Angle Orthod 72: 118–123.
4) Celikoglu M, Buyuk SK, Sekerci AE, Ucar FI (2014) Three-dimensional evaluation of the pharyngeal airway volumes in patients affected by unilateral cleft lip and palate. Am J Orthod Dentofacial Orthop 145: 780–786.
5) Cheung T, Oberoi S (2012) Three dimen-sional assessment of the pharyngeal airway in individuals with non-syndromic cleft lip and palate. PLOS ONE 7: e43405.
6) El H, Palomo JM (2013) Three-dimensional evaluation of upper airway following rapid maxillary expansion: A CBCT study. Angle Orthod 84: 265–273.
7) Jena AK, Singh SP, Utreja AK (2010) Sagittal mandibular development effects on the dimensions of the awake pharyngeal airway passage. Angle Orthod 80: 1061–1067.
8) Kim YJ, Hong JS, Hwang YI, Park YH (2010) Three-dimensional analysis of pharyngeal air-way in preadolescent children with different anteroposterior skeletal patterns. Am J Orthod Dentofacial Orthop 137: 306.e1–11.
9) Kuijpers-Jagman AM, Long Jr RE (2000) The influence of surgery and orthopedic treat-ment on maxillofacial growth and maxillary arch development in patients treated for oro-facial clefts. Cleft Palate Craniofac J 37: 1–12. 10) Kula K, Jeong AE, Stacey H, Kendall D,
different dental and skeletal malocclusions. J Biomed Graph Comput 3: 116.
11) Liao YF, Mars M (2005) Long-term effects of palate repair on craniofacial morphology in patients with unilateral cleft lip and palate. Cleft Palate Craniofac J 42: 594–600.
12) Muto T, Yamazaki A, Takeda S (2008) A cepha-lometric evaluation of the pharyngeal airway space in patients with mandibular retrogna-thia and prognaretrogna-thia, and normal subjects. Int J Oral Maxillofac Surg 37: 228–231.
13) Pimenta LA, de Rezende Barbosa GL, Pretti H, Emodi O, van Aalst J, Rossouw PE, Tyndall DA, Drake AF (2015) Three-dimensional evaluation of nasopharyngeal airways of uni-lateral cleft lip and palate patients. Laryngoscope 125: 736–739.
14) Rana SS, Duggal R, Kharbanda OP (2015) Area and volume of the pharyngeal airway in surgically treated unilateral cleft lip and palate patient: A cone beam computed tomography study. J Cleft Lip Palate Craniofacial Anomalies 2: 27–33.
15) Sheng CM, Lin LH, Su Y, Tsai HH (2009) Developmental changes in pharyngeal airway depth and hyoid bone position from child-hood to young adultchild-hood. Angle Orthod 79: 484–490.
16) Wermker K, Jung S, Joos U, Kleinheinz J (2012) Nasopharyngeal development in patients with cleft lip and palate: A retrospec-tive case-control study. Int J Otolaryngol 2012: 458–507.
17) Yoshihara M, Terajima M, Yanagita N, Hyakutake H, Kanomi R, Kitahara T, Takahashi I (2012) Three-dimensional analysis of the pharyngeal airway morphology in growing Japanese girls with and without cleft lip and palate. Am J Orthod Dentofacial Orthop 141: S92–S101.
18) Zhao Y, Nguyen M, Gohl E, Mah JK, Sameshima G, Enciso R (2010) Oropharyngeal airway changes after rapid palatal expansion evalu-ated with cone-beam computed tomography. Am J Orthod Dentofacial Orthop 137: S71– S78.
Correspondence:
Dr. Emiko Kimura
Department of Orthodontics, Tokyo Dental College,
1-2-2 Masago, Mihama-Ku, Chiba 261-8502, Japan
E-mail: [email protected]
tdc04-01_kimura.indd 219
